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Int J Syst Evol Microbiol 56 (2006), 443-448; DOI  10.1099/ijs.0.63942-0
© 2006 International Union of Microbiological Societies

Shinella granuli gen. nov., sp. nov., and proposal of the reclassification of Zoogloea ramigera ATCC 19623 as Shinella zoogloeoides sp. nov.

Dong-Shan An, Wan-Taek Im, Hee-Chan Yang and Sung-Taik Lee

Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Guseong-dong 373-1, Yuseong-gu, Daejeon 305-701, Republic of Korea

Correspondence
Sung-Taik Lee
e_stlee{at}kaist.ac.kr


   ABSTRACT
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The taxonomic position of a novel bacterial strain, Ch06T, isolated from an upflow anaerobic sludge blanket reactor was determined. Strain Ch06T was Gram-negative, aerobic, motile and oxidase- and catalase-positive. A comparative 16S rRNA gene sequence analysis showed a clear affiliation of strain Ch06T to the Alphaproteobacteria and it was most closely related to Zoogloea ramigera ATCC 19623 and Mycoplana dimorpha IAM 13154T (97·9 and 96·3 % sequence similarity, respectively). The major respiratory quinone was Q-10 and the predominant fatty acids were C16 : 0, 3-OH C16 : 0, C18 : 0, C19 : 0 cyclo {omega}8c and summed feature 7 (C18 : 1{omega}7c/{omega}9t/{omega}12t, C18 : 1{omega}7c/{omega}9c/{omega}12t). On the basis of phenotypic, chemotaxonomic and phylogenetic characteristics, the novel isolate was assigned to a new genus, Shinella gen. nov., as Shinella granuli gen. nov., sp. nov. (type strain Ch06T=KCTC 12237T=JCM 13254T). It is proposed that Zoogloea ramigera ATCC 19623 is reclassified into the novel genus Shinella as Shinella zoogloeoides sp. nov. (type strain ATCC 19623T=IAM 12669T=I-16-MT).

Abbreviations: UASB, upflow anaerobic sludge blanket

Published online ahead of print on 21 October 2005 as DOI 10.1099/ijs.0.63942-0.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain Ch06T is AY995149.


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In the course of a study on the culturable aerobic bacterial community in granules from an upflow anaerobic sludge blanket (UASB) reactor, a large number of novel bacterial strains were isolated (Bae et al., 2005Go; La et al., 2005Go). One of these isolates, designated Ch06T, occupied a distinct phylogenetic lineage with the previously described strain Zoogloea ramigera ATCC 19623 (=IAM 12669) within the ‘Rhizobiaceae group’ of the Alphaproteobacteria on the basis of 16S RNA gene sequence analysis.

Zoogloea ramigera, the type species of the genus Zoogloea (Unz, 1984Go), is defined as a Gram-negative, obligately aerobic, chemo-organotrophic, non-spore-forming, rod-shaped bacterium that produces a characteristic gelatinous matrix of finger-like projections, the so-called ‘zoogloeal matrix’ (Unz, 1984Go; Dugan et al., 1992Go). Three strains of Z. ramigera are well-known through a number of experimental studies: the type strain ATCC 19544T (=106T; Unz, 1971Go), ATCC 19623 (=I-16-M; Crabtree & McCoy, 1967Go) and ATCC 25935 (=P. R. Dugan 115; Dugan et al., 1992Go; Friedman & Dugan, 1968Go; Joyce & Dugan, 1970Go). The Z. ramigera type strain ATCC 19544T and strain ATCC 19623 are known to be different (Rosselló-Mora et al., 1993Go; Shin et al., 1993Go) and the third strain has been reclassified as the type strain of Duganella zoogloeoides (Hiraishi et al., 1997Go).

In this study, we report the results of a taxonomic examination of a newly isolated novel strain, Ch06T, and of strain ATCC 19623.

For the isolation of aerobic bacteria, brownish-black granules (around 2 mm in diameter) from a brewery wastewater-treating UASB reactor, which had been operated anaerobically for 2 years, were homogenized by using an Ace homogenizer (Nihonseiki). The suspension was spread on R2A agar plates (Difco) after being serially diluted with 50 mM phosphate buffer (pH 7·0). The plates were incubated at 30 °C for 2 weeks. Single colonies on the plates were purified by transferring them onto new plates and incubating them again under the same conditions. The purified colonies were tentatively identified by partial 16S rRNA gene sequences. Strain Ch06T was one of the isolates that appeared dominantly on the plates under aerobic conditions. After primary isolation and purification on R2A agar plates (Difco), strains were cultivated at 30 °C on the same medium and stored at –70 °C in R2A broth supplemented with 20 % (v/v) glycerol.

Extraction of genomic DNA, PCR-mediated amplification of the 16S rRNA gene and sequencing of the purified PCR product were carried out according to Kim et al. (2005)Go. The 16S rRNA gene sequences of related taxa were obtained from GenBank. Multiple alignments were performed using the CLUSTAL_X program (Thompson et al., 1997Go). Gaps were edited in the BioEdit program (Hall, 1999Go). Evolutionary distances were calculated using the Kimura two-parameter model (Kimura, 1983Go). Phylogenetic trees were constructed using the neighbour-joining (Saitou & Nei, 1987Go) and maximum-parsimony (Fitch, 1971Go) methods using the MEGA3 program (Kumar et al., 2004Go) with bootstrap values based on 1000 replications (Felsenstein, 1985Go).

Phylogenetic 16S rRNA gene sequence analyses indicated that strain Ch06T is a member of the family Rhizobiaceae and forms a distinct cluster with strain ATCC 19623 (Fig. 1Go). Genomic DNA of strain Ch06T was extracted and purified with the Qiagen genomic-tip system 100/G and was enzymically degraded into nucleosides as described by Mesbah et al. (1989)Go. The DNA G+C content was determined as described by Mesbah et al. (1989)Go using a reverse-phase HPLC. The DNA G+C content of strain Ch06T was 66 mol%. DNA–DNA hybridization was performed fluorometrically by the method of Ezaki et al. (1989)Go using photobiotin-labelled DNA probes and microdilution wells. The level of DNA–DNA relatedness between strains Ch06T and ATCC 19623 was 33 %, suggesting that the strains are different at the species level (Wayne et al., 1987Go; Stackebrandt & Goebel, 1994Go).


Figure 1
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  		Fig. 1. Rooted phylogenetic tree based on the 16S rRNA gene sequences of strain Ch06T and related bacteria in the Alphaproteobacteria. This tree was constructed using the neighbour-joining method (Saitou & Nei, 1987Go) with a Kimura (1983)Go two-parameter distance matrix and pairwise deletion. Dots indicate generic branches that were also recovered by using maximum-parsimony algorithms. Bootstrap values (expressed as percentages of 1000 replications) greater than 70 % are shown at the branch points. Bar, 0·02 substitutions per nucleotide position.

 
The cellular fatty acids of strain Ch06T, grown on trypticase soy agar (Difco) for 48 h, were saponified, methylated, extracted and identified by the Microbial Identification software package (Sasser, 1990Go). The major fatty acids of strain Ch06T were C16 : 0 (9·8–10·4 %), 3-OH C16 : 0 (1·6–2·2 %), C18 : 0 (1·6–2·6 %), C19 : 0 cyclo {omega}8c (3·0–4·9 %) and summed feature 7 (75·8–76·9 %; C18 : 1{omega}7c/{omega}9t/{omega}12t, C18 : 1{omega}7c/{omega}9c/{omega}12t), showing a similar pattern to those of strain ATCC 19623, except for the presence of summed feature 3 (C16 : 1{omega}7c/15 : 0 iso 2-OH) (Table 1Go). Respiratory lipoquinones were analysed as described previously (Komagata & Suzuki, 1987Go); the major respiratory lipoquinone was ubiquinone-10 (Q-10).


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  		Table 1. Cellular fatty acid profiles of strain Ch06T and type strains of related species

Species: 1, Shinella granuli sp. nov.; 2, Shinella zoogloeoides sp. nov.; 3, Mycoplana dimorpha; 4, Sinorhizobium fredii (data from Tighe et al., 2000Go); 5, Ochrobactrum anthropi (Trujillo et al., 2005Go). Fatty acids that account for <1·5 % of the total are not shown.

 
Cell morphology and motility were observed under a Nikon light microscope (x1000 magnification) with cells grown on R2A agar for 3 days at 28 °C. The presence of flagella was determined by transmission electron microscopy (JEM-10111; JEOL) after negative staining with uranyl acetate. Catalase activity was determined by bubble production in 3 % (v/v) H2O2 and oxidase activity was determined using 1 % (w/v) tetramethyl p-phenylenediamine. Growth at different temperatures and pH was assessed after 5 days incubation. Salt tolerance was tested on R2A medium supplemented with 1–10 % (w/v) NaCl after 5 days incubation. Growth was determined by monitoring the OD600. Anaerobic growth was observed in serum bottles by adding thioglycolate (1 g l–1) to R2A broth and substituting the upper air layer with nitrogen gas. Substrate utilization as the sole carbon source and some physiological characteristics were determined with API 32GN and API 20NE galleries according to the manufacturer's instructions (bioMérieux). Nitrate and nitrite reduction were confirmed by inoculating each strain into three 25 ml serum bottles containing 13 ml R2A medium. Nitrate and nitrite were added as KNO3 and NaNO2 at concentrations of 10 mM. The reduction of nitrate and nitrite was monitored by an ion chromatograph (790 personal IC; Metrohm) equipped with a conductivity detector and an anion exchange column (Metrosep Anion Supp 4; Metrohm). Nitrogen-fixing ability was determined by growth in 50 ml of a nitrogen-free medium (DSMZ medium no. 3) contained in a 500 ml Erlenmeyer flask. The primer system PolF–PolR (Poly et al., 2001Go) was used to amplify a nifH gene as described by Im et al. (2004)Go. DNA degradation [using DNA agar (Difco) supplemented with 0·01 % toluidine blue (Merck)], casein, cellulose and starch degradation (Atlas, 1993Go), lipid degradation (Kouker & Jaeger, 1987Go) and xylan degradation (Ten et al., 2004Go) were also investigated; reactions were read after 5 days. Duplicate antibiotic sensitivity tests were performed using filter paper discs containing the following: streptomycin (5, 10 and 15 µg ml–1), tetracycline (5, 10 and 15 µg–1), kanamycin (1·0, 1·5 and 2·0 mg ml–1) and ampicillin (20, 25 and 30 µg ml–1) (Sigma). Discs were placed on R2A plates spread with Ch06T culture and then incubated at 28 °C for 5 days.

Physiological, biochemical and morphological characteristics of the strains studied are listed under the species descriptions and are also given in Table 2Go. Phenotypic and chemotaxonomic examination shows that strains Ch06T and ATCC 19623 share many common characteristics. However, the strains differ with respect to nitrate reduction, growth at 40 °C, growth at 4 % NaCl, urease activity and their ability to assimilate carbon sources such as alanine, gluconate, 4-hydroxybenzoate, malate and salicin. Finally, the DNA–DNA relatedness value between the strains is low enough to differentiate them as separate species.


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  		Table 2. Comparison of selected characteristics of Shinella granuli Ch06T with those of its nearest phylogenetic neighbours within the ‘Rhizobiaceae group’

Species: 1, Shinella granuli sp. nov.; 2, Shinella zoogloeoides sp. nov.; 3, Mycoplana dimorpha; 4, Sinorhizobium fredii (data from de Lajudie et al., 1994Go; Wei et al., 2002Go; Willems et al., 2003Go; Young et al., 2001Go); 5, Ochrobactrum anthropi (de Lajudie et al., 1994Go; Lebuhn et al., 2000Go; Kämpfer et al., 2003Go; Trujillo et al., 2005Go). Data for taxa 1–3 are from this study. All strains were positive for assimilation of histidine, inositol, lactate, mannose, mannitol, proline and sorbitol and negative for assimilation of adipate, 3-hydroxybenzoate, suberate and phenylacetate and negative for gelatin hydrolysis. +, Positive; –, negative; W, weak.

 
Phylogenetically, the two strains form a novel lineage of descent within the Alphaproteobacteria which is clustered with Mycoplana dimorpha IAM 13154T (96·1–96·3 % similarity in 16S rRNA gene sequence) and Sinorhizobium fredii ATCC 35423T (95·2–95·5 % similarity). The phylogenetic divergence and low level of similarity between 16S rRNA gene sequences support the affiliation of strains Ch06T and ATCC 19623 into a novel genus. This is also supported by phenotypic and chemotaxonomic characteristics (Tables 1 and 2GoGo). The two strains can be differentiated from Mycoplana dimorpha IAM 13154T by beta-glucosidase and beta-galactosidase activity and the ability to assimilate arabinose, fucose, 2-ketogluconate, maltose, N-acetylglucosamine, propionate, L-rhamnose, D-ribose and sucrose. The hydroxy fatty acid identified for the two strains was 3-OH C16 : 0, which is a unique profile of the proposed new genus Shinella gen. nov., and different from those of other genera such as Mycoplana, Sinorhizobium and Ochrobactrum (Table 1Go). It is noted that, in some cases, this hydroxyl fatty acid is important for discriminating between genera, for example Sinorhizobium and Rhizobium (Tighe et al., 2000Go). Moreover, the absence of cellular fatty acid C17 : 0 also makes the genus Shinella different from the genera Mycoplana and Ochrobactrum (Table 1Go). Strains Ch06T and ATCC 19623 can be differentiated from Sinorhizobium fredii ATCC 35423T by nitrogen fixation and the ability to assimilate D-ribose and propionate. The DNA G+C content of strains Ch06T and ATCC 19623 was 2–4 mol% higher than that of Sinorhizobium (Table 2Go). Moreover, strains Ch06T and ATCC 19623 can be differentiated from Ochrobactrum anthropi LMG 3331T by their relatively low DNA G+C content and by their phenotypic and chemotaxonomic features (Tables 1 and 2GoGo). On the basis of morphological, phylogenetic, chemotaxonomic and physiological data, we propose that strain Ch06T is a member of a novel genus and species, Shinella granuli gen. nov., sp. nov. In addition, we propose the reclassification of Zoogloea ramigera ATCC 19623 to the genus Shinella as Shinella zoogloeoides sp. nov.

Description of Shinella gen. nov.
Shinella (Shi.nel'la. N.L. fem. dim. n. Shinella named after Yong-Kook Shin, for his contributions to reclassification of the genus Zoogloea).

Cells are Gram-negative, non-spore-forming, motile rods. Amorphous or finger-like flocculent growth occurs in liquid media. Catalase-, oxidase-, beta-galactosidase- and beta-glucosidase-positive. Predominant cellular fatty acids are C16 : 0 and summed feature 7 (C18 : 1{omega}7c/{omega}9t/{omega}12t, C18 : 1{omega}7c/{omega}9c/{omega}12t) and C16 : 0 3-OH is the predominant hydroxy fatty acid. The main lipoquinone is Q-10. DNA G+C content is 64–66 mol%. 16S rRNA gene sequence analysis indicates that the genus Shinella is a member of the family Rhizobiaceae of the Alphaproteobacteria. The type species is Shinella granuli.

Description of Shinella granuli sp. nov.
Shinella granuli (gra.nu'li. L. gen. n. granuli of a small grain, pertaining to a granule, from which the type strain was isolated).

Characteristics are as given for the genus. In addition, cells are 0·2–0·5 µm in width and 4–6 µm in length. Motile by means of multiple polar flagella (Fig. 2Go). Colonies on R2A agar media are glistening, convex with an entire margin, viscous and pale-yellow. Growth occurs at 4–40 °C, with 1–4 % NaCl and at pH 6–10. Nitrogen fixation is negative. Does not hydrolyse starch, cellulose, xylan, protein, lipid, casein, gelatin or DNA. Does not utilize adipate, arginine, caparate, citrate, glycogen, 3-hydroxybenzoate, itaconate, 2-ketogluconate, 5-ketogluconate, malonate, melibiose, phenylacetate, suberate or valerate as sole carbon sources. Resistant to 50 µg ampicillin ml–1 and 15 µg tetracycline ml–1, but sensitive to 5 µg streptomycin ml–1 and 1 mg kanamycin ml–1. The predominant cellular fatty acids are C16 : 0 (9·8–10·4 %), 3-OH C16 : 0 (1·6–2·2 %), C18 : 0 (1·6–2·6 %), C19 : 0 cyclo {omega}8c (3·0–4·9 %) and summed feature 7 (75·8–76·9 %; C18 : 1{omega}7c/{omega}9t/{omega}12t, C18 : 1{omega}7c/{omega}9c/{omega}12t). The major respiratory quinone is Q-10. DNA G+C content is 66 mol%.


Figure 2
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  		Fig. 2. Transmission electron micrograph of a motile cell of Shinella granuli Ch06T. Bar, 1 µm.

 
The type strain, Ch06T (=KCTC 12237T=JCM 13254T), was isolated from a UASB reactor.

Description of Shinella zoogloeoides sp. nov.
Shinella zoogloeoides (zoo.gloe.o'i.des. N.L. n. Zoogloea bacterial genus name; Gr. suff. -oides similar to; N.L. adj. zoogloeoides similar to Zoogloea).

The description is as given for the genus and by Shin et al. (1993)Go and Rosselló-Mora et al. (1993)Go, with the addition that it is negative in tests for amylase, protease, lipase, cellulose, xylanase, DNase, gelatinase and urease. Nitrogen fixation is negative. Does not utilize adipate, alanine, arginine, caparate, citrate, glycogen, gluconate, 3-hydroxybenzoate, 4-hydroxybenzoate, itaconate, 2-ketogluconate, 5-ketogluconate, malate, malonate, melibiose, phenylacetate, salicin, suberate or valerate. The predominant cellular fatty acids are C16 : 0 (13·4 %), 3-OH C16 : 0 (8·1 %), C18 : 0 (2·6 %), C19 : 0 cyclo {omega}8c (2·9 %) and summed feature 7 (72·9 %; C18 : 1{omega}7c/{omega}9t/{omega}12t, C18 : 1{omega}7c/{omega}9c/{omega}12t). The major respiratory quinone is Q-10. DNA G+C content is 64 mol%.

The type strain, ATCC 19623T (=IAM 12669T=I-16-MT), was isolated from sewage treatment systems.


   ACKNOWLEDGEMENTS
 
This work was supported by the 21C Frontier Microbial Genomics and Application Center Program, Ministry of Science & Technology (grant MG05-0101-4-0) and by Eco-Tecnopia-21, Ministry of Environment, Republic of Korea.


   REFERENCES
TOP
 ABSTRACT
 MAIN TEXT
 REFERENCES
 
Atlas, R. M. (1993). Handbook of Microbiological Media. Edited by L. C. Parks. Boca Raton, FL: CRC Press.

Bae, H.-S., Im, W.-T. & Lee, S.-T. (2005). Lysobacter concretionis sp. nov., isolated from anaerobic granules in an upflow anaerobic sludge blanket reactor. Int J Syst Evol Microbiol 55, 1155–1161.[Abstract/Free Full Text]

Crabtree, K. & McCoy, E. (1967). Zoogloea ramigera Itzigsohn, identification and description. Request for an Opinion as to the status of the generic name Zoogloea. Int J Syst Bacteriol 17, 1–10.

de Lajudie, P., Willems, A., Pot, B. & 7 other authors (1994). Polyphasic taxonomy of Rhizobia: emendation of the genus Sinorhizobium and description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov., and Sinorhizobium teranga sp. nov. Int J Syst Bacteriol 44, 715–733.[CrossRef]

Dugan, P. R., Stoner, D. L. & Pickrum, H. M. (1992). The genus Zoogloea. In The Prokaryotes, 2nd edn, pp. 3952–3964. Edited by A. Balows, H. G. Trüper, M. Dworkin, W. Harder & K.-H. Schleifer. New York: Springer.

Ezaki, T., Hashimoto, Y. & Yabuuchi, E. (1989). Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39, 224–229.[CrossRef]

Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.[CrossRef]

Fitch, W. M. (1971). Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20, 406–416.[CrossRef]

Friedman, B. A. & Dugan, P. R. (1968). Identification of Zoogloea species and the relationship to zoogloeal matrix and floc formation. J Bacteriol 95, 1903–1909.[Abstract/Free Full Text]

Hall, T. A. (1999). BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41, 95–98.

Hiraishi, A., Shin, Y. K. & Sugiyama, J. (1997). Proposal to reclassify Zoogloea ramigera IAM 12670 (P. R. Dugan 115) as Duganella zoogloeoides gen. nov., sp. nov. Int J Syst Bacteriol 47, 1249–1252.[CrossRef][Medline]

Im, W.-T., Bae, H.-S., Yokota, A. & Lee, S. T. (2004). Herbaspirillum chlorophenolicum sp. nov., a 4-chlorophenol-degrading bacterium. Int J Syst Evol Microbiol 54, 851–855.[Abstract/Free Full Text]

Joyce, G. H. & Dugan, P. R. (1970). The role of floc-forming bacteria in BOD removal from wastewater. Dev Ind Microbiol 11, 377–386.

Kämpfer, P., Buczolits, S., Albrecht, A., Busse, H.-J. & Stackebrandt, E. (2003). Towards a standardized format for the description of a novel species (of an established genus): Ochrobactrum gallinifaecis sp. nov. Int J Syst Evol Microbiol 53, 893–896.[Abstract/Free Full Text]

Kim, M. K., Im, W.-T., Ohta, H., Lee, M. & Lee, S.-T. (2005). Sphingopyxis granuli sp. nov., a beta-glucosidase-producing bacterium in the family Sphingomonadaceae in {alpha}-4 subclass of the Proteobacteria. J Microbiol 43, 152–157.[Medline]

Kimura, M. (1983). The Neutral Theory of Molecular Evolution, pp. 41–46. Cambridge: Cambridge University Press.

Komagata, K. & Suzuki, K. (1987). Lipid and cell wall analysis in bacterial systematics. Methods Microbiol 19, 161–207.

Kouker, G. & Jaeger, K.-E. (1987). Specific and sensitive plate assay for bacterial lipases. Appl Environ Microbiol 53, 211–213.[Abstract/Free Full Text]

Kumar, S., Tamura, K. & Nei, M. (2004). MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5, 150–163.[Abstract/Free Full Text]

La, H.-J., Im, W.-T., Ten, L. N., Kang, M.-S., Shin, D.-Y. & Lee, S.-T. (2005). Paracoccus koreensis sp. nov., isolated from anaerobic granules in an upflow anaerobic sludge blanket (UASB) reactor. Int J Syst Evol Microbiol 55, 1657–1660.[Abstract/Free Full Text]

Lebuhn, M., Achouak, W., Schloter, M., Berge, O., Meier, H., Barakat, M., Hartmann, A. & Heulin, T. (2000). Taxonomic characterization of Ochrobactrum sp. isolates from soil samples and wheat roots, and description of Ochrobactrum tritici sp. nov. and Ochrobactrum grignonense sp. nov. Int J Syst Evol Microbiol 50, 2207–2223.[Abstract]

Mesbah, M., Premachandran, U. & Whitman, W. B. (1989). Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39, 159–167.

Poly, F., Monrozier, L. J. & Bally, R. (2001). Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152, 95–103.[Medline]

Rosselló-Mora, R. A., Ludwig, W. & Schleifer, K. H. (1993). Zoogloea ramigera: a phylogenetically diverse species. FEMS Microbiol Lett 114, 129–134.

Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.[Abstract]

Sasser, M. (1990). Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids. MIDI Technical Note 101. Newark, DE: MIDI Inc.

Shin, Y. K., Hiraishi, A. & Sugiyama, J. (1993). Molecular systematics of the genus Zoogloea and emendation of the genus. Int J Syst Bacteriol 43, 826–831.[CrossRef][Medline]

Stackebrandt, E. & Goebel, B. M. (1994). Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44, 846–849.[CrossRef]

Ten, L. N., Im, W.-T., Kim, M.-K., Kang, M.-S. & Lee, S.-T. (2004). Development of a plate technique for screening of polysaccharide-degrading microorganisms by using a mixture of insoluble chromogenic substrates. J Microbiol Methods 56, 375–382.[CrossRef][Medline]

Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[Abstract/Free Full Text]

Tighe, S. W., de Lajudie, P., Dipietro, K., Lindström, K., Nick, G. & Jarvis, B. D. W. (2000). Analysis of cellular fatty acids and phenotypic relationships of Agrobacterium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium species using the Sherlock Microbial Identification System. Int J Syst Evol Microbiol 50, 787–801.[Abstract]

Trujillo, M. E., Willems, A., Abril, A., Planchuelo, A. M., Rivas, R., Ludeña, D., Mateos, P. F., Martínez-Molina, E. & Velázquez, E. (2005). Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol 71, 1318–1327.[Abstract/Free Full Text]

Unz, R. F. (1971). Neotype strain of Zoogloea ramigera Itzigsohn. Request for an Opinion. Int J Syst Bacteriol 21, 91–99.

Unz, R. F. (1984). Genus IV. Zoogloea Itzigsohn 1868, 30AL. In Bergey's Manual of Systematic Bacteriology, vol. 1, pp. 214–219. Edited by N. R. Krieg & J. G. Holt. Baltimore: Williams & Wilkins.

Wayne, L. G., Brenner, D. J., Colwell, R. R. & 9 other authors (1987). International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37, 463–464.[CrossRef]

Wei, G. H., Wang, E. T., Tan, Z. Y., Zhu, M. E. & Chen, W. X. (2002). Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulacea. Int J Syst Evol Microbiol 52, 2231–2239.[Abstract]

Willems, A., Fernández-López, M., Muñoz-Adelantado, E., Goris, J., De Vos, P., Martínez-Romero, E., Toro, N. & Gillis, M. (2003). Description of new Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Casida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an Opinion. Int J Syst Evol Microbiol 53, 1207–1217.[Abstract/Free Full Text]

Young, J. M., Kuykendall, L. D., Martínez-Romero, E., Kerr, A. & Sawada, H. (2001). A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol 51, 89–103.[Abstract]




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Shinella kummerowiae sp. nov., a symbiotic bacterium isolated from root nodules of the herbal legume Kummerowia stipulacea
Int J Syst Evol Microbiol, June 1, 2008; 58(6): 1409 - 1413.
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 Int. J. Syst. Evol. Microbiol.Home page
H.-W. Lee, H.-S. Yu, Q.-m. Liu, H.-M. Jung, D.-S. An, W.-T. Im, F.-X. Jin, and S.-T. Lee
Kaistia granuli sp. nov., isolated from anaerobic granules in an upflow anaerobic sludge blanket reactor
Int J Syst Evol Microbiol, October 1, 2007; 57(10): 2280 - 2283.
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 Int. J. Syst. Evol. Microbiol.Home page
W.-T. Im, Z. Aslam, M. Lee, L. N. Ten, D.-C. Yang, and S.-T. Lee
Starkeya koreensis sp. nov., isolated from rice straw.
Int J Syst Evol Microbiol, October 1, 2006; 56(Pt 10): 2409 - 2414.
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